Changes in the photoreceptor mosaic of P23H-1 rats during retinal degeneration: Implications for rod-cone dependent survival

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 8, 2013, Pages 5888-5900

  García Ayuso, Diego ^a   Ortín Martínez, Arturo ^a   Jiménez López, Manuel ^a   Galindo Romero, Caridad ^a   Cuenca, Nicolás ^b   Pinilla, Isabel ^c   Vidal Sanz, Manuel ^a   Agudo Barriuso, Marta ^a,d   Villegas Pérez, María P ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b UNIVERSITY OF ALICANTE   (Spain)

^c HOSPITAL CLÍNICO UNIVERSITARIO LOZANO BLESA   (Spain)

^d HOSPITAL UNIVERSITARIO VIRGEN DE LA ARRIXACA   (Spain)

Author keywords

Automated quantification; Opsin; P23H; Retinitis pigmentosa; Rhodopsin; Rings

Indexed keywords

OPSIN; RECOVERIN; RHODOPSIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENSITY; FEMALE; IMAGE ANALYSIS; IMMUNODETECTION; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA CONE; RETINA ROD; RETINITIS PIGMENTOSA; TOPOGRAPHY;

AUTOMATED QUANTIFICATION; OPSIN; P23H; RETINITIS PIGMENTOSA; RHODOPSIN; RINGS;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOHISTOCHEMISTRY; OPSINS; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL DEGENERATION; RETINAL ROD PHOTORECEPTOR CELLS; RHODOPSIN;

EID: 84883224029     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-12643     Document Type: Article

References (72)

1. Daiger SP, Sullivan LS, Bowne SJ. RetNet: The Retinal Information Network. Available at: http://www.sph.uth.tmc. edu/RetNet. Accessed June 19, 2013.
2. Pacione LR, Szego MJ, Ikeda S, Nishina PM, McInnes RR. Progress toward understanding the genetic and biochemical mechanisms of inherited photoreceptor degenerations. Annu Rev Neurosci. 2003;26:657-700.
3. Ayuso C, Millan JM. Retinitis pigmentosa and allied conditions today: a paradigm of translational research. Genome Med. 2010;2:34.
4. Cepko CL. Emerging gene therapies for retinal degenerations. J Neurosci. 2012;32:6415-6420.
5. Milam AH, Li ZY, Fariss RN. Histopathology of the human retina in retinitis pigmentosa. Prog Retin Eye Res. 1998;17: 175-205.
6. LaVail MM, Yasumura D, Matthes MT, et al. Ribozyme rescue of photoreceptor cells in P23H transgenic rats: long-term survival and late-stage therapy. Proc Natl Acad Sci U S A. 2000;97: 11488-11493.
7. Lewin AS, Drenser KA, Hauswirth WW, et al. Ribozyme rescue of photoreceptor cells in a transgenic rat model of autosomal dominant retinitis pigmentosa. Nat Med. 1998;4:967-971.
8. Machida S, Kondo M, Jamison JA, et al. P23H rhodopsin transgenic rat: correlation of retinal function with histopathology. Invest Ophthalmol Vis Sci. 2000;41:3200-3209.
9. Steinberg RH, Flannery JG, Naash M, et al. Transgenic rat models of inherited retinal degeneration caused by mutant opsin genes. Invest Ophthalmol Vis Sci. 1996;37:S698.
10. Dryja TP, McGee TL, Reichel E, et al. A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature. 1990;25:364-366.
11. Wang S, Lu B, Lund RD. Morphological changes in the Royal College of Surgeons rat retina during photoreceptor degeneration and after cell based therapy. J Comp Neurol. 2005;491: 400-417.
12. Ferrari S, Di Iorio E, Barbaro V, Ponzin D, Sorrentino FS, Parmeggiani F. Retinitis pigmentosa: genes and disease mechanisms. Curr Genomics. 2011;12:238-249.
13. Chrysostomou V, Valter K, Stone J. Cone-rod dependence in the rat retina: variation with the rate of rod damage. Invest Ophthalmol Vis Sci. 2009;50:3017-3023.
14. Chrysostomou V, Stone J, Valter K. Life history of cones in the rhodopsin mutant P23H-3 rat: evidence of long-term survival. Invest Ophthalmol Vis Sci. 2009;50:2407-2416.
15. Léveillard T, Mohand-Saïd S, Lorentz O, et al. Identification and characterization of rod-derived cone viability factor. Nat Genet. 2004;36:755-759.
16. Stone J, Maslim J, Valter-Kocsi K, et al. Mechanisms of photoreceptor death and survival in mammalian retina. Prog Retin Eye Res. 1999;18:689-735.
17. Marc RE, Jones BW. Retinal remodeling in inherited photoreceptor degenerations. Mol Neurobiol. 2003;28:139-147.
18. Marc RE, Jones BW, Watt CB, Strettoi E. Neural remodeling in retinal degeneration. Prog Retin Eye Res. 2003;22:607-655.
19. Ripps H. Cell death in retinitis pigmentosa: gap junctions and the 'bystander' effect. Exp Eye Res. 2002;74:327-336.
20. Chrysostomou V, Stone J, Stowe S, Barnett NL, Valter K. The status of cones in the rhodopsin mutant P23H-3 retina: lightregulated damage and repair in parallel with rods. Invest Ophthalmol Vis Sci. 2008;49:1116-1125.
21. Hartong DT, Berson EL, Dryja TP. Retinitis pigmentosa. Lancet. 2006;368:1795-1809.
22. John SK, Smith JE, Aguirre GD, Milam AH. Loss of cone molecular markers in rhodopsin-mutant human retinas with retinitis pigmentosa. Mol Vis. 2000;6:204-215.
23. LaVail MM, Matthes MT, Yasumura D, Steinberg RH. Variability in rate of cone degeneration in the retinal degeneration (rd/rd) mouse. Exp Eye Res. 1997;65:45-50.
24. Lin B, Masland RH, Strettoi E. Remodeling of cone photoreceptor cells after rod degeneration in rd mice. Exp Eye Res. 2009;88:589-599.
25. Punzo C, Kornacker K, Cepko CL. Stimulation of the insulin/ mTOR pathway delays cone death in a mouse model of retinitis pigmentosa. Nat Neurosci. 2009;12:44-52.
26. Marc RE, Jones BW, Anderson JR, et al. Neural reprogramming in retinal degeneration. Invest Ophthalmol Vis Sci. 2007;48: 3364-3371.
27. Pinilla I, Lund RD, Sauvé Y. Enhanced cone dysfunction in rats homozygous for the P23H rhodopsin mutation. Neurosci Lett. 2005;382:16-21.
28. Lu B, Morgans CW, Girman S, Lund R, Wang S. Retinal morphological and functional changes in an animal model of retinitis pigmentosa. Vis Neurosci. 2013;19:1-13.
29. Hombrebueno JR, Tsai MM, Kim HL, De Juan J, Grzywacz NM, Lee EJ. Morphological changes of short-wavelength cones in the developing S334ter-3 transgenic rat. Brain Res. 2010; 1321:60-66.
30. Li Y, Tao W, Luo L, et al. CNTF induces regeneration of cone outer segments in a rat model of retinal degeneration. PLoS One. 2010;5:e9495.
31. Xia X, Li Y, Huang D, et al. Oncostatin M protects rod and cone photoreceptors and promotes regeneration of cone outer segment in a rat model of retinal degeneration. PLoS One. 2011;6:e18282.
32. Ji Y, Zhu CL, Grzywacz NM, Lee EJ. Rearrangement of the cone mosaic in the retina of the rat model of retinitis pigmentosa. J Comp Neurol. 2012;520:874-888.
33. García-Ayuso D, Salinas-Navarro M, Agudo M, et al. Retinal ganglion cell numbers and delayed retinal ganglion cell death in the P23H rat retina. Exp Eye Res. 2010;91:800-810.
34. Ortín-Martínez A, Jiménez-López M, Nadal-Nicolás FM, et al. Automated quantification and topographical distribution of the whole population of S-and L-cones in adult albino and pigmented rats. Invest Ophthalmol Vis Sci. 2010;51:3171-3183.
35. García-Ayuso D, Salinas-Navarro M, Agudo-Barriuso M, Alarcón-Martínez L, Vidal-Sanz M, Villegas-Pérez MP. Retinal ganglion cell axonal compression by retinal vessels in light-induced retinal degeneration. Mol Vis. 2011;17:1716-1733.
36. Nadal-Nicolás FM, Jimenez-Lopez M, Sobrado-Calvo P, et al. Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naïve and optic nerve injured retinas. Invest Ophthalmol Vis Sci. 2009;50:3860-3868.
37. Fernández-Sánchez L, Lax P, Esquiva G, Martín-Nieto J, Pinilla I, Cuenca N. Safranal, a saffron constituent, attenuates retinal degeneration in P23H rats. PLoS One. 2012;7:e43074.
38. Lafuente López-Herrera MP, Mayor-Torroglosa S, Miralles de Imperial J, Villegas-Pérez MP, Vidal-Sanz M. Transient ischemia of the retina results in altered retrograde axoplasmic transport: neuroprotection with brimonidine. Exp Neurol. 2002;178: 243-258.
39. Nadal-Nicolás FM, Jiménez-López M, Salinas-Navarro M, et al. Whole number, distribution and co-expression of brn3 transcription factors in retinal ganglion cells of adult albino and pigmented rats. PLoS One. 2012;7:e49830.
40. Salinas-Navarro M, Mayor-Torroglosa S, Jiménez-López M, et al. A computerized analysis of the entire retinal ganglion cell population and its spatial distribution in adult rats. Vis Res. 2009;49:115-126.
41. Salinas-Navarro M, Alarcón-Martínez L, Valiente-Soriano FJ, et al. Ocular hypertension impairs optic nerve axonal transport leading to progressive retinal ganglion cell degeneration. Exp Eye Res. 2010;90:168-183.
42. Vidal-Sanz M, Lafuente MP, Mayor S, Miralles de Imperial J, Villegas-Pérez MP. Retinal ganglion cell death induced by retinal ischemia: neuroprotective effects of two alpha-2 agonists. Surv Ophthalmol. 2001;45:261-267.
43. Cuenca N, Pinilla I, Sauvé Y, Lu B, Wang S, Lund RD. Regressive and reactive changes in the connectivity patterns of rod and cone pathways of P23H transgenic rat retina. Neuroscience. 2004;127:301-317.
44. Martínez-Navarrete GC, Seiler MJ, Aramant RB, Fernández-Sanchéz L, Pinilla I, Cuenca N. Retinal degeneration in two lines of transgenic S334ter rats. Exp Eye Res. 2011;92:227-237.
45. Lee DC, Vazquez-Chona FR, Ferrell WD, et al. Dysmorphic photoreceptors in a P23H mutant rhodopsin model of retinitis pigmentosa are metabolically active and capable of regenerating to reverse retinal degeneration. J Neurosci. 2012;32:2121-2128.
46. Haeri M, Knox BE. Rhodopsin mutant P23H destabilizes rod photoreceptor disk membranes. PLoS One. 2012;7:e30101.
47. Malanson KM, Lem J. Rhodopsin-mediated retinitis pigmentosa. Prog Mol Biol Transl Sci. 2009;88:1-31.
48. LaVail MM. Analysis of neurological mutants with inherited retinal degeneration. Friedenwald lecture. Invest Ophthalmol Vis Sci. 1981;21:638-657.
49. Szel A, Rohlich P. Two cone types of rat retina detected by antivisual pigment antibodies. Exp Eye Res. 1992;55:47-52.
50. LaVail MM. Survival of some photoreceptor cells in albino rats following long-term exposure to continuous light. Invest Ophthalmol. 1976;15:64-70.
51. Yu DY, Cringle S, Valter K, Walsh N, Lee D, Stone J. Photoreceptor death, trophic factor expression, retinal oxygen status, and photoreceptor function in the P23H rat. Invest Ophthalmol Vis Sci. 2004;45:2013-2019.
52. Williams RW. The human retina has a cone-enriched rim. Vis Neurosci. 1991;6:403-406.
53. Mollon JD, Regan BC, Bowmaker JK. What is the function of the cone-rich rim of the retina? Eye. 1998;12:548-552.
54. Vugler A, Semo M, Joseph A, Jeffery G. Survival and remodeling of melanopsin cells during retinal dystrophy. Vis Neurosci. 2008;25:125-138.
55. Martínez-Navarrete GC, Angulo A. Martín-Nieto J, Cuenca N. Gradual morphogenesis of retinal neurons in the peripheral retinal margin of adult monkeys and humans. J Comp Neurol. 2008;511:557-580.
56. Fischer AJ, Reh TA. Growth factors induce neurogenesis in the ciliary body. Dev Biol. 2003;259:225-240.
57. Mayer EJ, Hughes EH, Carter DA, Dick AD. Nestin positive cells in adult human retina and in epiretinal membranes. Br J Ophthalmol. 2003;87:1154-1158.
58. Moshiri A, Reh TA. Persistent progenitors at the retinal margin of ptc+/-mice. J Neurosci. 2004;24:229-237.
59. Fei, Y. Cone neurite sprouting: an early onset abnormality of the cone photoreceptors in the retinal degeneration mouse. Mol Vis. 2002;8:306-314.
60. Morris AC, Schroeter EH, Bilotta J, Wong RO, Fadool JM. Cone survival despite rod degeneration in XOPS-mCFP transgenic zebrafish. Invest Ophthalmol Vis Sci. 2005;46:4762-4271.
61. Yang Y, Mohand-Said S, Léveillard T, Fontaine V, Simonutti M, Sahel JA. Transplantation of photoreceptor and total neural retina preserves cone function in P23H rhodopsin transgenicrat. PLoS One. 2010;5:e13469.
62. Zhu CL, Ji Y, Lee EJ, Grzywacz NM. Spatiotemporal pattern of rod degeneration in the S334ter-line-3 rat model of retinitis pigmentosa. Cell Tissue Res. 2013;351:29-40.
63. Liu C, Li Y, Peng M, Laties AM, Wen R. Activation of caspase-3 in the retina of transgenic rats with the rhodopsin mutation s334ter during photoreceptor degeneration. J Neurosci. 1999; 19:4778-4485.
64. Kaur J, Mencl S, Sahaboglu A, et al. Calpain and PARP activation during photoreceptor cell death in P23H and S334ter rhodopsin mutant rats. PLoS One. 2011;6:e22181.
65. Marco-Gomariz MA, Hurtado-Montalbán N, Vidal-Sanz M, Lund RD, Villegas-Pérez MP. Phototoxic-induced photoreceptor degeneration causes retinal ganglion cell degeneration in pigmented rats. J Comp Neurol. 2006;498:163-179.
66. Marc RE, Jones BW, Watt CB, Vazquez-Chona F, Vaughan DK, Organisciak DT. Extreme retinal remodeling triggered by light damage: implications for age related macular degeneration. Mol Vis. 2008;14:782-806.
67. Vaughan DK, Coulibaly SF, Darrow RM, Organisciak DT. A morphometric study of light-induced damage in transgenic rat models of retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2003;44:848-855.
68. Clarke G, Collins RA, Leavitt BR, et al. A one-hit model of cell death in inherited neuronal degenerations. Nature. 2000;406: 195-199.
69. Edward DP, Lim K, Sawaguchi S, Tso MO. An immunohistochemical study of opsin in photoreceptor cells following lightinduced retinal degeneration in the rat. Graefes Arch Clin Exp Ophthalmol. 1993;231:289-294.
70. Nir I, Agarwal N, Sagie G, Papermaster DS. Opsin distribution and synthesis in degenerating photoreceptors of rd mutant mice. Exp Eye Res. 1989;49:403-421.
71. Nir I, Papermaster DS. Immunocytochemical localization of opsin in degenerating photoreceptors of RCS rats and rd and rds mice. Prog Clin Biol Res. 1989;314:251-264.
72. Li ZY, Kljavin IJ, Milam AH. Rod photoreceptor neurite sprouting in retinitis pigmentosa. J Neurosci. 1995;15:5429-5438.